Heterotrimeric G proteins directly regulate MMP14/membrane type-1 matrix metalloprotease:A novel mechanism for GPCR-EGFR transactivation

Journal of Biological Chemistry

Volumn 290, Issue 16, 2015, Pages 9941-9947

  Overland, Aaron C ^a   Insel, Paul A ^a  

^a UNIVERSITY OF SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CHEMICAL ACTIVATION; MEMBRANES; RECOMBINANT PROTEINS;

DIRECT ACTIVATION; EPIDERMAL GROWTH FACTOR RECEPTORS; EPIDERMAL GROWTH FACTORS; G PROTEIN ACTIVATION; G PROTEIN COUPLED RECEPTORS; HETEROTRIMERIC G PROTEINS; MATRIX METALLOPROTEASE; PEPTIDE INHIBITORS;

PROTEINS;

EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; PHOSPHOLIPASE C; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; ANGIOTENSIN II; EGFR PROTEIN, RAT; ENZYME INHIBITOR; GALLEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE TRIPHOSPHATE; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; PERTUSSIS TOXIN; PHENYLEPHRINE; SMALL INTERFERING RNA; XANTHENE DERIVATIVE;

ADULT; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME RELEASE; ENZYME SPECIFICITY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RAT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSACTIVATION; 3T3 CELL LINE; ANIMAL; CELL MEMBRANE; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; GENETICS; HEART MUSCLE CELL; METABOLISM; MOUSE; PRIMARY CELL CULTURE; PROTEIN MULTIMERIZATION; SECRETION (PROCESS); SPRAGUE DAWLEY RAT; TRANSCRIPTION INITIATION;

RATTUS;

ANGIOTENSIN II; ANIMALS; CELL MEMBRANE; ENZYME INHIBITORS; FIBROBLASTS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); GUANOSINE TRIPHOSPHATE; HEPARIN-BINDING EGF-LIKE GROWTH FACTOR; MALE; MATRIX METALLOPROTEINASE 14; MICE; MYOCYTES, CARDIAC; NIH 3T3 CELLS; PERTUSSIS TOXIN; PHENYLEPHRINE; PRIMARY CELL CULTURE; PROTEIN MULTIMERIZATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; XANTHENES;

EID: 84927924551     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C115.647073     Document Type: Article

References (45)

1. Gschwind, A., Zwick, E., Prenzel, N., Leserer, M., and Ullrich, A. (2001) Cell communication networks: epidermal growth factor receptor transactivation as the paradigm for interreceptor signal transmission. Oncogene 20, 1594-1600
2. Rozengurt, E. (2007) Mitogenic signaling pathways induced by G protein-coupled receptors. J. Cell. Physiol. 213, 589-602
3. Spinale, F. G. (2007) Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 87, 1285-1342
4. Holmbeck, K., Bianco, P., Yamada, S., and Birkedal-Hansen, H. (2004) MT1-MMP: a tethered collagenase. J. Cell. Physiol. 200, 11-19
5. Itoh, Y. (2006) MT1-MMP: a key regulator of cell migration in tissue. IUBMB Life 58, 589-596
6. Arroyo, A. G., Genís, L., Gonzalo, P., Matías-Román, S., Pollán, A., and Gálvez, B. G. (2007) Matrix metalloproteinases: new routes to the use of MT1-MMP as a therapeutic target in angiogenesis-related disease. Curr. Pharm. Des. 13, 1787-1802
7. Gingras, D., and Béliveau, R. (2010) Emerging concepts in the regulation of membrane-type 1 matrix metalloproteinase activity. Biochim. Biophys. Acta 1803, 142-150
8. Strongin, A. Y. (2010) Proteolytic and non-proteolytic roles of membrane type-1 matrix metalloproteinase in malignancy. Biochim. Biophys. Acta 1803, 133-141
9. Sato, H., and Takino, T. (2010) Coordinate action of membrane-type matrix metalloproteinase-1 (MT1-MMP) and MMP-2 enhances pericellular proteolysis and invasion. Cancer Sci. 101, 843-847
10. Sounni, N. E., Paye, A., Host, L., and Noël, A. (2011) MT-MMPS as regulators of vessel stability associated with angiogenesis. Front. Pharmacol. 2, 111
11. Turner, N. A., and Porter, K. E. (2012) Regulation of myocardial matrix metalloproteinase expression and activity by cardiac fibroblasts. IUBMB Life 64, 143-150
12. Spinale, F. G., Janicki, J. S., and Zile, M. R. (2013) Membrane-associated matrix proteolysis and heart failure. Circ. Res. 112, 195-208
13. Shah, B. H., Yesilkaya, A., Olivares-Reyes, J. A., Chen, H. D., Hunyady, L., and Catt, K. J. (2004) Differential pathways of angiotensin II-induced extracellularly regulated kinase 1/2 phosphorylation in specific cell types: role of heparin-binding epidermal growth factor. Mol. Endocrinol. 18, 2035-2048
14. Shah, B. H., Shah, F. B., and Catt, K. J. (2006) Role of metalloproteinase-dependent EGF receptor activation in α-adrenoceptor-stimulated MAP kinase phosphorylation in GT1-7 neurons. J. Neurochem. 96, 520-532
15. Belcheva, M. M., Szúcs, M., Wang, D., Sadee, W., and Coscia, C. J. (2001) μ-Opioid receptor-mediated ERK activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J. Biol. Chem. 276, 33847-33853
16. Ohtsu, H., Dempsey, P. J., and Eguchi, S. (2006) ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 291, C1-10
17. Daub, H., Weiss, F. U., Wallasch, C., and Ullrich, A. (1996) Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379, 557-560
18. Daub, H., Wallasch, C., Lankenau, A., Herrlich, A., and Ullrich, A. (1997) Signal characteristics of G protein-transactivated EGF receptor. EMBO J. 16, 7032-7044
19. Noma, T., Lemaire, A., Naga Prasad, S. V., Barki-Harrington, L., Tilley, D. G., Chen, J., Le Corvoisier, P., Violin, J. D., Wei, H., Lefkowitz, R. J., and Rockman, H. A. (2007) β-Arrestin-mediated β1-adrenergic receptor transactivation of the EGFR confers cardioprotection. J. Clin. Invest. 117, 2445-2458
20. Kim, J., Ahn, S., Rajagopal, K., and Lefkowitz, R. J. (2009) Independent β-arrestin2 and Gq/protein kinase Cζ pathways for ERK stimulated by angiotensin type 1A receptors in vascular smooth muscle cells converge on transactivation of the epidermal growth factor receptor. J. Biol. Chem. 284, 11953-11962
21. Bokemeyer, D., Schmitz, U., and Kramer, H. J. (2000) Angiotensin II-induced growth of vascular smooth muscle cells requires an Src-dependent activation of the epidermal growth factor receptor. Kidney Int. 58, 549-558
22. Amorino, G. P., Deeble, P. D., and Parsons, S. J. (2007) Neurotensin stimulates mitogenesis of prostate cancer cells through a novel c-Src/Stat5b pathway. Oncogene 26, 745-756
23. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., and Ullrich, A. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888
24. Miyamoto, S., Hirata, M., Yamazaki, A., Kageyama, T., Hasuwa, H., Mizushima, H., Tanaka, Y., Yagi, H., Sonoda, K., Kai, M., Kanoh, H., Nakano, H., and Mekada, E. (2004) Heparin-binding EGF-like growth factor is a promising target for ovarian cancer therapy. Cancer Res. 64, 5720-5727
25. Yokoyama, U., Patel, H. H., Lai, N. C., Aroonsakool, N., Roth, D. M., and Insel, P. A. (2008) The cyclic AMP effector Epac integrates pro- and antifibrotic signals. Proc. Natl. Acad. Sci. U.S.A. 105, 6386-6391
26. Suojanen, J., Salo, T., Koivunen, E., Sorsa, T., and Pirilä, E. (2009) A novel and selective membrane type-1 matrix metalloproteinase (MT1-MMP) inhibitor reduces cancer cell motility and tumor growth. Cancer Biol. Ther. 8, 2362-2370
27. Smith, N. J., Chan, H. W., Osborne, J. E., Thomas, W. G., and Hannan, R. D. (2004) Hijacking epidermal growth factor receptors by angiotensin II: new possibilities for understanding and treating cardiac hypertrophy. Cell. Mol. Life Sci. 61, 2695-2703
28. Prenzel, N., Fischer, O. M., Streit, S., Hart, S., and Ullrich, A. (2001) The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr. Relat. Cancer 8, 11-31
29. Daaka, Y., Luttrell, L. M., and Lefkowitz, R. J. (1997) Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature 390, 88-91
30. Luttrell, L. M., Della Rocca, G. J., van Biesen, T., Luttrell, D. K., and Lefkowitz, R. J. (1997) Gβγ subunits mediate Src-dependent phosphorylation of the epidermal growth factor receptor: a scaffold for G protein-coupled receptor-mediated Ras activation. J. Biol. Chem. 272, 4637-4644
31. Mahajan, R., Ha, J., Zhang, M., Kawano, T., Kozasa, T., and Logothetis, D. E. (2013) A computational model predicts that Gβγ acts at a cleft between channel subunits to activate GIRK1 channels. Sci. Signal. 6, ra69
32. Schwindinger, W. F., and Robishaw, J. D. (2001) Heterotrimeric G-protein βγ-dimers in growth and differentiation. Oncogene 20, 1653-1660
33. Castagliuolo, I., Valenick, L., Liu, J., and Pothoulakis, C. (2000) Epidermal growth factor receptor transactivation mediates substance P-induced mitogenic responses in U-373 MG cells. J. Biol. Chem. 275, 26545-26550
34. Rusinova, R., Mirshahi, T., and Logothetis, D. E. (2007) Specificity of Gβγsignaling to Kir3 channels depends on the helical domain of pertussis toxin-sensitive Gα subunits. J. Biol. Chem. 282, 34019-34030
35. Arribas, J., Coodly, L., Vollmer, P., Kishimoto, T. K., Rose-John, S., and Massagué, J. (1996) Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors. J. Biol. Chem. 271, 11376-11382
36. Dempsey, P. J., Meise, K. S., Yoshitake, Y., Nishikawa, K., and Coffey, R. J. (1997) Apical enrichment of human EGF precursor in Madin-Darby canine kidney cells involves preferential basolateral ectodomain cleavage sensitive to a metalloprotease inhibitor. J. Cell Biol. 138, 747-758
37. Brown, C. L., Meise, K. S., Plowman, G. D., Coffey, R. J., and Dempsey, P. J. (1998) Cell surface ectodomain cleavage of human amphiregulin precursor is sensitive to a metalloprotease inhibitor. Release of a predominant N-glycosylated 43-kDa soluble form. J. Biol. Chem. 273, 17258-17268
38. Ouyang, M., Huang, H., Shaner, N. C., Remacle, A. G., Shiryaev, S. A., Strongin, A. Y., Tsien, R. Y., and Wang, Y. (2010) Simultaneous visualization of protumorigenic Src and MT1-MMP activities with fluorescence resonance energy transfer. Cancer Res. 70, 2204-2212
39. Uchiyama-Tanaka, Y., Matsubara, H., Mori, Y., Kosaki, A., Kishimoto, N., Amano, K., Higashiyama, S., and Iwasaka, T. (2002) Involvement of HB-EGF and EGF receptor transactivation in TGF-β-mediated fibronectin expression in mesangial cells. Kidney Int. 62, 799-808
40. Thomas, W. G., Brandenburger, Y., Autelitano, D. J., Pham, T., Qian, H., and Hannan, R. D. (2002) Adenoviral-directed expression of the type 1A angiotensin receptor promotes cardiomyocyte hypertrophy via transactivation of the epidermal growth factor receptor. Circ. Res. 90, 135-142
41. Luttrell, L. M., Hawes, B. E., van Biesen, T., Luttrell, D. K., Lansing, T. J., and Lefkowitz, R. J. (1996) Role of c-Src tyrosine kinase in G protein-coupled receptor- and Gβγ subunit-mediated activation of mitogen-activated protein kinases. J. Biol. Chem. 271, 19443-19450
42. Nishihara, T., Remacle, A. G., Angert, M., Shubayev, I., Shiryaev, S. A., Liu, H., Dolkas, J., Chernov, A. V., Strongin, A. Y., and Shubayev, V. I. (2015) Matrix Metalloproteinase-14 both sheds cell surface neuronal glial antigen 2 (NG2) proteoglycan on macrophages and governs the response to peripheral nerve injury. J. Biol. Chem. 290, 3693-3707
43. Huang, S. M., and Harari, P. M. (1999) Epidermal growth factor receptor inhibition in cancer therapy: biology, rationale and preliminary clinical results. Invest. New Drugs 17, 259-269
44. Olayioye, M. A., Neve, R. M., Lane, H. A., and Hynes, N. E. (2000) The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 19, 3159-3167
45. Rossé, C., Lodillinsky, C., Fuhrmann, L., Nourieh, M., Monteiro, P., Irondelle, M., Lagoutte, E., Vacher, S., Waharte, F., Paul-Gilloteaux, P., Romao, M., Sengmanivong, L., Linch, M., van Lint, J., Raposo, G., Vincent-Salomon, A., Bièche, I., Parker, P. J., and Chavrier, P. (2014) Control of MT1-MMP transport by atypical PKC during breast-cancer progression. Proc. Natl. Acad. Sci. U.S.A. 111, E1872-E1879